Activation of PAR2 receptors sensitizes primary afferents and causes leukocyte rolling and adherence in the rat knee joint

British Journal of Pharmacology

Volumn 167, Issue 8, 2012, Pages 1665-1678

  Russell, F A ^a   Schuelert, N ^a   Veldhoen, V E ^a   Hollenberg, M D ^a   McDougall, J J ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

inflammation; joint pain; leukocyte accumulation; PAR2

Indexed keywords

2 [1 IMINO 2 (2 METHOXYPHENYL)ETHYL] 7,7 DIPHENYLPERHYDROISOINDOL 4 ONE; 4 CHLORO N (3 METHOXYPHENYL)CINNAMAMIDE; FLUOROGOLD; NEUROKININ 1 RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 2; VANILLOID RECEPTOR 1;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; INTRAVITAL MICROSCOPY; KNEE ARTHRITIS; LEUKOCYTE ADHERENCE; LEUKOCYTE ROLLING; MALE; MICROSCOPY; NERVE FIBER; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NERVOUS SYSTEM PARAMETERS; NONHUMAN; PATHOPHYSIOLOGY; PRIMARY AFFERENT SENSITIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SPINAL GANGLION; SYNOVIUM;

ANILIDES; ANIMALS; ARTHRITIS; CELL ADHESION; CINNAMATES; ISOINDOLES; KNEE JOINT; LEUKOCYTE ROLLING; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS, AFFERENT; OLIGOPEPTIDES; RATS; RATS, WISTAR; RECEPTOR, PAR-2; RECEPTORS, NEUROKININ-1; TRPV CATION CHANNELS;

EID: 84870510938     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.02120.x     Document Type: Article

References (55)

1. Adams MN, Ramachandran R, Yau MK, Suen JY, Fairlie DP, Hollenberg MD, et al,. (2011). Structure, function and pathophysiology of protease activated receptors. Pharmacol Ther 130: 248-282.
2. Al-Ani B, Saifeddine M, Kawabata A, Renaux B, Mokashi S, Hollenberg MD, (1999). Proteinase-activated receptor 2 (PAR(2)): development of a ligand-binding assay correlating with activation of PAR(2) by PAR(1)- and PAR(2)-derived peptide ligands. J Pharmacol Exp Ther 290: 753-760.
3. Alexander SPH, Mathie A, Peters JA, (2011). Guide to Receptors and Channels (GRAC), 5th edn. Br J Pharmacol 164 (Suppl. 1): S1-S324.
4. Alier KA, Endicott JA, Stemkowski PL, Cenac N, Cellars L, Chapman K, et al,. (2008). Intrathecal administration of proteinase-activated receptor-2 agonists produces hyperalgesia by exciting the cell bodies of primary sensory neurons. J Pharmacol Exp Ther 324: 224-233.
5. Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisani M, et al,. (2004). Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 24: 4300-4312.
6. Amadesi S, Cottrell GS, Divino L, Chapman K, Grady EF, Bautista F, et al,. (2006). Protease-activated receptor 2 sensitizes TRPV1 by protein kinase Cepsilon- and A-dependent mechanisms in rats and mice. J Physiol 575: 555-571.
7. Andruski B, McCafferty DM, Ignacy T, Millen B, McDougall JJ, (2008). Leukocyte trafficking and pain behavioral responses to a hydrogen sulfide donor in acute monoarthritis. Am J Physiol Regul Integr Comp Physiol 295: R814-R820.
8. Bohm SK, Khitin LM, Grady EF, Aponte G, Payan DG, Bunnett NW, (1996). Mechanisms of desensitization and resensitization of proteinase-activated receptor-2. J Biol Chem 271: 22003-22016.
9. Brierley SM, Castro J, Harrington AM, Hughes PA, Page AJ, Rychkov GY, et al,. (2011). TRPA1 contributes to specific mechanically activated currents and sensory neuron mechanical hypersensitivity. J Physiol 589: 3575-3593.
10. Busso N, Frasnelli M, Feifel R, Cenni B, Steinhoff M, Hamilton J, et al,. (2007). Evaluation of protease-activated receptor 2 in murine models of arthritis. Arthritis Rheum 56: 101-107.
11. Cao T, Pinter E, Al Rashed S, Gerard N, Hoult JR, Brain SD, (2000). Neurokinin-1 receptor agonists are involved in mediating neutrophil accumulation in the inflamed, but not normal, cutaneous microvasculature: an in vivo study using neurokinin-1 receptor knockout mice. J Immunol 164: 5424-5429.
12. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, et al,. (2000). Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288: 306-313.
13. Coelho AM, Vergnolle N, Guiard B, Fioramonti J, Bueno L, (2002). Proteinases and proteinase-activated receptor 2: a possible role to promote visceral hyperalgesia in rats. Gastroenterology 122: 1035-1047.
14. Costa R, Marotta DM, Manjavachi MN, Fernandes ES, Lima-Garcia JF, Paszcuk AF, et al,. (2008). Evidence for the role of neurogenic inflammation components in trypsin-elicited scratching behaviour in mice. Br J Pharmacol 154: 1094-1103.
15. Cui M, Honore P, Zhong C, Gauvin D, Mikusa J, Hernandez G, et al,. (2006). TRPV1 receptors in the CNS play a key role in broad-spectrum analgesia of TRPV1 antagonists. J Neurosci 26: 9385-9393.
16. Dai Y, Moriyama T, Higashi T, Togashi K, Kobayashi K, Yamanaka H, et al,. (2004). Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci 24: 4293-4299.
17. Dai Y, Wang S, Tominaga M, Yamamoto S, Fukuoka T, Higashi T, et al,. (2007). Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 117: 1979-1987.
18. Damiano BP, Cheung WM, Santulli RJ, Fung-Leung WP, Ngo K, Ye RD, et al,. (1999). Cardiovascular responses mediated by protease-activated receptor-2 (PAR-2) and thrombin receptor (PAR-1) are distinguished in mice deficient in PAR-2 or PAR-1. J Pharmacol Exp Ther 288: 671-678.
19. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, et al,. (2000). Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405: 183-187.
20. Fernandes ES, Russell FA, Spina D, McDougall JJ, Graepel R, Gentry C, et al,. (2011). A distinct role for TRPA1, in addition to TRPV1, in TNFalpha-induced inflammatory hyperalgesia and CFA-induced mono-arthritis. Arthritis Rheum 63: 819-829.
21. Ferrell WR, Lockhart JC, Kelso EB, Dunning L, Plevin R, Meek SE, et al,. (2003). Essential role for proteinase-activated receptor-2 in arthritis. J Clin Invest 111: 35-41.
22. Ferrell WR, Kelso EB, Lockhart JC, Plevin R, McInnes IB, (2010). Protease-activated receptor 2: a novel pathogenic pathway in a murine model of osteoarthritis. Ann Rheum Dis 69: 2051-2054.
23. Grant AD, Cottrell GS, Amadesi S, Trevisani M, Nicoletti P, Materazzi S, et al,. (2007). Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J Physiol 578: 715-733.
24. Hansen KK, Sherman PM, Cellars L, Andrade-Gordon P, Pan Z, Baruch A, et al,. (2005). A major role for proteolytic activity and proteinase-activated receptor-2 in the pathogenesis of infectious colitis. Proc Natl Acad Sci USA 102: 8363-8368.
25. Harrington AM, Hughes PA, Martin CM, Yang J, Castro J, Isaacs NJ, et al,. (2011). A novel role for TRPM8 in visceral afferent function. Pain 152: 1459-1468.
26. Helyes Z, Sandor K, Borbely E, Tekus V, Pinter E, Elekes K, et al,. (2010). Involvement of transient receptor potential vanilloid 1 receptors in protease-activated receptor-2-induced joint inflammation and nociception. Eur J Pain 14: 351-358.
27. Hollenberg MD, Compton SJ, (2002). International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol Rev 54: 203-217.
28. Hollenberg MD, Renaux B, Hyun E, Houle S, Vergnolle N, Saifeddine M, et al,. (2008). Derivatized 2-furoyl-LIGRLO-amide, a versatile and selective probe for proteinase-activated receptor 2: binding and visualization. J Pharmacol Exp Ther 326: 453-462.
29. Ivanavicius SP, Blake DR, Chessell IP, Mapp PI, (2004). Isolectin B4 binding neurons are not present in the rat knee joint. Neuroscience 128: 555-560.
30. Kanai Y, Nakazato E, Fujiuchi A, Hara T, Imai A, (2005). Involvement of an increased spinal TRPV1 sensitization through its up-regulation in mechanical allodynia of CCI rats. Neuropharmacology 49: 977-984.
31. Kawabata A, Kawao N, Kuroda R, Tanaka A, Itoh H, Nishikawa H, (2001). Peripheral PAR-2 triggers thermal hyperalgesia and nociceptive responses in rats. Neuroreport 12: 715-719.
32. Kawabata A, Kanke T, Yonezawa D, Ishiki T, Saka M, Kabeya M, et al,. (2004). Potent and metabolically stable agonists for protease-activated receptor-2: evaluation of activity in multiple assay systems in vitro and in vivo. J Pharmacol Exp Ther 309: 1098-1107.
33. Kelso EB, Lockhart JC, Hembrough T, Dunning L, Plevin R, Hollenberg MD, et al,. (2006). Therapeutic promise of proteinase-activated receptor-2 antagonism in joint inflammation. J Pharmacol Exp Ther 316: 1017-1024.
34. Li Z, Proud D, Zhang C, Wiehler S, McDougall JJ, (2005). Chronic arthritis down-regulates peripheral mu-opioid receptor expression with concomitant loss of endomorphin 1 antinociception. Arthritis Rheum 52: 3210-3219.
35. Lindner JR, Kahn ML, Coughlin SR, Sambrano GR, Schauble E, Bernstein D, et al,. (2000). Delayed onset of inflammation in protease-activated receptor-2-deficient mice. J Immunol 165: 6504-6510.
36. McDougall JJ, (2011). Peripheral analgesia: hitting pain where it hurts. Biochim Biophys Acta 1812: 459-467.
37. McDougall JJ, Hanesch U, Pawlak M, Schmidt RF, (2001). Participation of NK1 receptors in nociceptin-induced modulation of rat knee joint mechanosensitivity. Exp Brain Res 137: 249-253.
38. McGrath J, Drummond G, Kilkenny C, Wainwright C, (2010). Guidelines for reportingexperiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
39. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R, (2001). Proteinase-activated receptors. Pharmacol Rev 53: 245-282.
40. Miyazaki Y, Satoh T, Nishioka K, Yokozeki H, (2006). STAT-6-mediated control of P-selectin by substance P and interleukin-4 in human dermal endothelial cells. Am J Pathol 169: 697-707.
41. Nakano S, Mishiro T, Takahara S, Yokoi H, Hamada D, Yukata K, et al,. (2007). Distinct expression of mast cell tryptase and protease activated receptor-2 in synovia of rheumatoid arthritis and osteoarthritis. Clin Rheumatol 26: 1284-1292.
42. Oikonomopoulou K, Hansen KK, Saifeddine M, Tea I, Blaber M, Blaber SI, et al,. (2006). Proteinase-activated receptors, targets for kallikrein signaling. J Biol Chem 281: 32095-32112.
43. Ramachandran R, Hollenberg MD, (2008). Proteinases and signalling: pathophysiological and therapeutic implications via PARs and more. Br J Pharmacol 153 (Suppl. 1): S263-S282.
44. Richardson JD, Vasko MR, (2002). Cellular mechanisms of neurogenic inflammation. J Pharmacol Exp Ther 302: 839-845.
45. Russell FA, McDougall JJ, (2009). Proteinase activated receptor (PAR) involvement in mediating arthritis pain and inflammation. Inflamm Res 58: 119-126.
46. Russell FA, Veldhoen VE, Tchitchkan D, McDougall JJ, (2010). Proteinase-activated receptor-4 (PAR4) activation leads to sensitization of rat joint primary afferents via a bradykinin B2 receptor-dependent mechanism. J Neurophysiol 103: 155-163.
47. Russell FA, Zhan S, Dumas A, Lagarde S, Pouliot M, McDougall JJ, (2011). The pronociceptive effect of proteinase-activated receptor-4 stimulation in rat knee joints is dependent on mast cell activation. Pain 152: 354-360.
48. Salo PT, Theriault E, (1997). Number, distribution and neuropeptide content of rat knee joint afferents. J Anat 190: 515-522.
49. Schuelert N, McDougall JJ, (2008). Cannabinoid-mediated antinociception is enhanced in rat osteoarthritic knees. Arthritis Rheum 58: 145-153.
50. Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, Ennes HS, et al,. (2000). Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 6: 151-158.
51. Varga A, Nemeth J, Szabo A, McDougall JJ, Zhang C, Elekes K, et al,. (2005). Effects of the novel TRPV1 receptor antagonist SB366791 in vitro and in vivo in the rat. Neurosci Lett 385: 137-142.
52. Vergnolle N, Hollenberg MD, Sharkey KA, Wallace JL, (1999). Characterization of the inflammatory response to proteinase-activated receptor-2 (PAR2)-activating peptides in the rat paw. Br J Pharmacol 127: 1083-1090.
53. Vergnolle N, Bunnett NW, Sharkey KA, Brussee V, Compton SJ, Grady EF, et al,. (2001). Proteinase-activated receptor-2 and hyperalgesia: a novel pain pathway. Nat Med 7: 821-826.
54. Yang YH, Hall P, Little CB, Fosang AJ, Milenkovski G, Santos L, et al,. (2005). Reduction of arthritis severity in protease-activated receptor-deficient mice. Arthritis Rheum 52: 1325-1332.
55. Zhang H, Cang CL, Kawasaki Y, Liang LL, Zhang YQ, Ji RR, et al,. (2007). Neurokinin-1 receptor enhances TRPV1 activity in primary sensory neurons via PKCepsilon: a novel pathway for heathyperalgesia. J Neurosci 27: 12067-12077.